Key Points
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Chemotaxis allows bacteria to swim towards environments that are better for growth. The process is involved in pathogenicity, biofilm formation and the establishment of symbiotic relationships.
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Changes in attractant and repellent concentrations are detected by clusters of chemoreceptors. Bacteria can sense very small changes in attractant concentration over a wide range of background concentrations.
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The chemoreceptor clusters control the activity of a two-component system comprising the histidine protein kinase CheA and the response regulators CheY and CheB. Phosphorylated CheY controls flagellar motor switching, whereas phosphorylated CheB mediates adaptation.
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The Escherichia coli chemotaxis signalling pathway is one of the simplest and best understood, but it is becoming increasingly apparent that most bacteria have more complex chemosensory pathways involving multiple homologues of the E. coli chemotaxis proteins.
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Rhodobacter sphaeroides has one of the best understood complex chemotaxis pathways; it has two distinct types of chemosensory cluster: one that is positioned at the cell pole and detects changes in the external attractant and repellent concentrations, and another that is cytoplasmic and is believed to monitor the metabolic state of the cell (a form of energy taxis).
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Structural studies have revealed the specificity determinants in the interaction of CheY proteins with CheA proteins and allowed rewiring of the signalling pathway. Mechanisms of signal integration and signal termination have been elucidated by mathematical modelling.
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Some bacteria have complex chemotaxis pathways that go beyond what is found in E. coli and R. sphaeroides. For example, in addition to the methylation-based adaptation system, Bacillus subtilis has two further adaptation pathways, one involving CheC and CheD and another using CheV.
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Some bacteria exploit the ability of the chemotaxis circuitry to sense small changes in ligand concentrations, and use the system to control behaviour other than chemotaxis. For example, Myxococcus xanthus has a chemotaxis-like pathway controlling development of the fruiting body, and Pseudomonas aeruginosa has one controlling biofilm formation.
Abstract
Bacteria use chemotaxis to migrate towards environments that are better for growth. Chemoreceptors detect changes in attractant levels and signal through two-component systems to control swimming direction. This basic pathway is conserved across all chemotactic bacteria and archaea; however, recent work combining systems biology and genome sequencing has started to elucidate the additional complexity of the process in many bacterial species. This article focuses on one of the best understood complex networks, which is found in Rhodobacter sphaeroides and integrates sensory data about the external environment and the metabolic state of the cell to produce a balanced response at the flagellar motor.
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References
Williams, S. M. et al. Helicobacter pylori chemotaxis modulates inflammation and bacterium-gastric epithelium interactions in infected mice. Infect. Immun. 75, 3747–3757 (2007).
Garvis, S. et al. Caenorhabditis elegans semi-automated liquid screen reveals a specialized role for the chemotaxis gene cheB2 in Pseudomonas aeruginosa virulence. PLoS Pathog. 5, e1000540 (2009).
Greer-Phillips, S. E., Stephens, B. B. & Alexandre, G. An energy taxis transducer oromotes root colonization by Azospirillum brasilense. J. Bacteriol. 186, 6595–6604 (2004).
Miller, L. D., Yost, C. K., Hynes, M. F. & Alexandre, G. The major chemotaxis gene cluster of Rhizobium leguminosarum bv. viciae is essential for competitive nodulation. Mol. Microbiol. 63, 348–362 (2007).
Berg, H. C. Bacterial flagellar motor. Curr. Biol. 18, R689–R691 (2008).
Armitage, J. P., Pitta, T. P., Vigeant, M. A., Packer, H. L. & Ford, R. M. Transformations in flagellar structure of Rhodobacter sphaeroides and possible relationship to changes in swimming speed. J. Bacteriol. 181, 4825–4833 (1999).
Hazelbauer, G. L., Falke, J. J. & Parkinson, J. S. Bacterial chemoreceptors: high-performance signaling in networked arrays. Trends Biochem. Sci. 33, 9–19 (2008). An excellent review of chemoreceptor structure and function.
Alexander, R. P. & Zhulin, I. B. Evolutionary genomics reveals conserved structural determinants of signaling and adaptation in microbial chemoreceptors. Proc. Natl Acad. Sci. USA 104, 2885–2890 (2007).
Wadhams, G. H. & Armitage, J. P. Making sense of it all: bacterial chemotaxis. Nature Rev. Mol. Cell. Biol. 5, 1024–1037 (2004).
Amin, D. N. & Hazelbauer, G. L. The chemoreceptor dimer is the unit of conformational coupling and transmembrane signaling. J. Bacteriol. 192, 1193–1200 (2010).
Parkinson, J. S. Signaling mechanisms of HAMP domains in chemoreceptors and sensor kinases. Annu. Rev. Microbiol. 64, 101–122 (2010).
Maddock, J. R. & Shapiro, L. Polar location of the chemoreceptor complex in the Escherichia coli cell. Science 259, 1717–1723 (1993).
Briegel, A. et al. Universal architecture of bacterial chemoreceptor arrays. Proc. Natl Acad. Sci. USA 106, 17181–17186 (2009). A detailed cryotomography study showing that bacterial chemoreceptor arrays have a conserved structure in a diverse range of species.
Bray, D., Levin, M. D. & Morton, F. C. Receptor clustering as a cellular mechanism to control sensitivity. Nature 393, 85–88 (1998). A modelling paper that uses chemoreceptor coupling within clusters to explain sensitivity and gain.
Goldman, J. P., Levin, M. D. & Bray, D. Signal amplification in a lattice of coupled protein kinases. Mol. Biosyst. 5, 1853–1859 (2009). A recent modelling paper suggesting that signal amplification may happen at the level of CheA within the chemoreceptor array.
Sourjik, V. & Berg, H. C. Receptor sensitivity in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 99, 123–127 (2002).
Endres, R. G. et al. Variable sizes of Escherichia coli chemoreceptor signaling teams. Mol. Syst. Biol. 4, 211 (2008).
Segall, J. E., Block, S. M. & Berg, H. C. Temporal comparisons in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 83, 8987–8991 (1986).
Borkovich, K. A. & Simon, M. I. The dynamics of protein phosphorylation in bacterial chemotaxis. Cell 63, 1339–1348 (1990).
Dyer, C. M., Vartanian, A. S., Zhou, H. & Dahlquist, F. W. A molecular mechanism of bacterial flagellar motor switching. J. Mol. Biol. 388, 71–84 (2009).
Sarkar, M. K., Paul, K. & Blair, D. Chemotaxis signaling protein CheY binds to the rotor protein FliN to control the direction of flagellar rotation in Escherichia coli. Proc. Natl Acad. Sci. USA 107, 9370–9375 (2010).
Welch, M., Oosawa, K., Aizawa, S.-I. & Eisenbach, M. Phosphorylation-dependent binding of a signal molecule to the flagellar switch of bacteria. Proc. Natl Acad. Sci. USA 90, 8787–8791 (1993).
Delalez, N. J. et al. Signal-dependent turnover of the bacterial flagellar switch protein FliM. Proc. Natl Acad. Sci. USA 107, 11347–11351 (2010).
Bai, F. et al. Conformational spread as a mechanism for cooperativity in the bacterial flagellar switch. Science 327, 685–689 (2010).
Thomas, D. R., Morgan, D. G. & DeRosier, D. J. Rotational symmetry of the C ring and a mechanism for the flagellar rotary motor. Proc. Natl Acad. Sci. USA 96, 10134–10139 (1999).
Cluzel, P., Surette, M. & Leibler, S. An ultrasensitive bacterial motor revealed by monitoring signaling proteins in single cells. Science 287, 1652–1655 (2000).
Silversmith, R. E. Auxiliary phosphatases in two-component signal transduction. Curr. Opin. Microbiol. 13, 177–183 (2010). A comprehensive review of the diverse family of phosphatases involved in two-component systems.
Vladimirov, N. & Sourjik, V. Chemotaxis: how bacteria use memory. Biol. Chem. 390, 1097–1104 (2009).
Anand, G. S. & Stock, A. M. Kinetic basis for the stimulatory effect of phosphorylation on the methylesterase activity of CheB. Biochemistry 41, 6752–6760 (2002).
Rao, C. V., Glekas, G. D. & Ordal, G. W. The three adaptation systems of Bacillus subtilis chemotaxis. Trends Microbiol. 16, 480–487 (2008).
Schweinitzer, T. & Josenhans, C. Bacterial energy taxis: a global strategy? Arch. Microbiol. 192, 507–520 (2010).
Porter, S. L., Wadhams, G. H. & Armitage, J. P. Rhodobacter sphaeroides: complexity in chemotactic signalling. Trends Microbiol. 16, 251–260 (2008).
Hamer, R., Chen, P.-Y., Armitage, J. P., Reinert, G. & Deane, C. M. Deciphering chemotaxis pathways using cross species comparisons. BMC Syst. Biol. 4, 3 (2010).
Wuichet, K. & Zhulin, I. B. Origins and diversification of a complex signal transduction system in prokaryotes. Sci. Signal. 3, ra50 (2010). A detailed genomics survey of the chemotaxis pathways of sequenced bacterial species.
Nicholls, D. G. & Ferguson, S. J. Bioenergetics 3 (Academic, London, 2009).
Slovak, P. M., Wadhams, G. H. & Armitage, J. P. Localization of MreB in Rhodobacter sphaeroides under conditions causing changes in cell shape and membrane structure. J. Bacteriol. 187, 54–64 (2005).
Slovak, P. M., Porter, S. L. & Armitage, J. P. Differential localization of Mre proteins with PBP2 in Rhodobacter sphaeroides. J. Bacteriol. 188, 1691–1700 (2006).
Gauden, D. E. & Armitage, J. P. Electron transport-dependent taxis in Rhodobacter sphaeroides. J. Bacteriol. 177, 5853–5859 (1995).
Jeziore-Sassoon, Y., Hamblin, P. A., Bootle, W. C., Poole, P. S. & Armitage, J. P. Metabolism is required for chemotaxis to sugars in Rhodobacter sphaeroides. Microbiology 144, 229–239 (1998).
Ingham, C. J. & Armitage, J. P. Involvement of transport in Rhodobacter sphaeroides chemotaxis. J. Bacteriol. 169, 5801–5807 (1987).
Grishanin, R. N., Gauden, D. E. & Armitage, J. P. Photoresponses in Rhodobacter sphaeroides: role of photosynthetic electron transport. J. Bacteriol. 179, 24–30 (1997).
Alexandre, G., Greer-Phillips, S. & Zhulin, I. B. Ecological role of energy taxis in microorganisms. FEMS Microbiol. Rev. 28, 113–126 (2004).
Xie, Z., Ulrich, L. E., Zhulin, I. & Alexandre, G. PAS domain containing chemoreceptor couples dynamic changes in metabolism with chemotaxis. Proc. Natl Acad. Sci. USA 107, 2235–2240 (2010).
Taylor, B. L., Zhulin, I. B. & Johnson, M. S. Aerotaxis and other energy-sensing behavior in bacteria. Annu. Rev. Microbiol. 53, 103–128 (1999).
Shah, D. S. et al. Identification of a fourth cheY gene in Rhodobacter sphaeroides and interspecies interaction within the bacterial chemotaxis signal transduction pathway. Mol. Microbiol. 35, 101–112 (2000).
Shah, D. S. H., Porter, S. L., Martin, A. C., Hamblin, P. A. & Armitage, J. P. Fine tuning bacterial chemotaxis: analysis of Rhodobacter sphaeroides behaviour under aerobic and anaerobic conditions by mutation of the major chemotaxis operons and cheY genes. EMBO J. 19, 4601–4613 (2000).
Porter, S. L., Warren, A. V., Martin, A. C. & Armitage, J. P. The third chemotaxis locus of Rhodobacter sphaeroides is essential for chemotaxis. Mol. Microbiol. 46, 1081–1094 (2002).
Hamblin, P. A., Maguire, B. A., Grishanin, R. N. & Armitage, J. P. Evidence for two chemosensory pathways in Rhodobacter sphaeroides. Mol. Microbiol. 26, 1083–1096 (1997).
Mackenzie, C. et al. The home stretch, a first analysis of the nearly completed genome of Rhodobacter sphaeroides 2.4.1. Photosynth. Res. 70, 19–41 (2001).
Poggio, S. et al. A complete set of flagellar genes acquired by horizontal transfer coexists with the endogenous flagellar system in Rhodobacter sphaeroides. J. Bacteriol. 189, 3208–3216 (2007). An ingenious study using suppressor mutants to isolate a motile R. sphaeroides strain expressing the Fla2 flagellum from a non-motile Fla1− parent strain.
Kobayashi, K. et al. Purification and characterization of the flagellar basal body of Rhodobacter sphaeroides. J. Bacteriol. 185, 5295–5300 (2003).
Shah, D. S., Perehinec, T., Stevens, S. M., Aizawa, S. I. & Sockett, R. E. The flagellar filament of Rhodobacter sphaeroides: pH-induced polymorphic transitions and analysis of the fliC gene. J. Bacteriol. 182, 5218–5224 (2000).
Armitage, J. P. & Macnab, R. M. Unidirectional intermittent rotation of the flagellum of Rhodobacter sphaeroides. J. Bacteriol. 169, 514–518 (1987).
del Campo, A. M. et al. Chemotactic control of the two flagellar systems of Rhodobacter sphaeroides is mediated by different sets of CheY and FliM proteins. J. Bacteriol. 189, 8397–8401 (2007).
McCarter, L. The multiple identities of Vibrio parahaemolyticus. J. Mol. Microbiol. Biotechnol. 1, 51–57 (1999).
McClain, J., Rollo, D. R., Rushing, B. G. & Bauer, C. E. Rhodospirillum centenum utilizes separate motor and switch components to control lateral and polar flagellum rotation. J. Bacteriol. 184, 2429–2438 (2002).
Kojima, M., Kubo, R., Yakushi, T., Homma, M. & Kawagishi, I. The bidirectional polar and unidirectional lateral flagellar motors of Vibrio alginolyticus are controlled by a single CheY species. Mol. Microbiol. 64, 57–67 (2007).
Mackenzie, C. et al. Postgenomic adventures with Rhodobacter sphaeroides. Annu. Rev. Microbiol. 61, 283–307 (2007).
Aldridge, P. & Hughes, K. T. Regulation of flagellar assembly. Curr. Opin. Microbiol. 5, 160–165 (2002).
Pena-Sanchez, J. et al. Identification of the binding site of the σ54 hetero-oligomeric FleQ/FleT activator in the flagellar promoters of Rhodobacter sphaeroides. Microbiology 155, 1669–1679 (2009).
Poggio, S., Osorio, A., Dreyfus, G. & Camarena, L. The flagellar hierarchy of Rhodobacter sphaeroides is controlled by the concerted action of two enhancer-binding proteins. Mol. Microbiol. 58, 969–983 (2005).
Poggio, S., Osorio, A., Dreyfus, G. & Camarena, L. The four different σ54 factors of Rhodobacter sphaeroides are not functionally interchangeable. Mol. Microbiol. 46, 75–85 (2002).
Martin, A. C., Gould, M., Byles, E., Roberts, M. A. J. & Armitage, J. P. Two chemosensory operons of Rhodobacter sphaeroides are regulated independently by sigma 28 and sigma 54. J. Bacteriol. 188, 7932–7940 (2006).
Arai, H., Roh, J. H. & Kaplan, S. Transcriptome dynamics during the transition from anaerobic photosynthesis to aerobic respiration in Rhodobacter sphaeroides 2.4.1. J. Bacteriol. 190, 286–299 (2008).
Pilizota, T. et al. A molecular brake, not a clutch, stops the Rhodobacter sphaeroides flagellar motor. Proc. Natl Acad. Sci. USA 106, 11582–11587 (2009).
Lloyd, S. A. & Blair, D. F. Charged residues of the rotor protein FliG essential for torque generation in the flagellar motor of Escherichia coli. J. Mol. Biol. 266, 733–744 (1997).
Lee, L. K., Ginsburg, M. A., Crovace, C., Donohoe, M. & Stock, D. Structure of the torque ring of the flagellar motor and the molecular basis for rotational switching. Nature 466, 996–1000 (2010).
Morehouse, K. A., Goodfellow, I. G. & Sockett, R. E. A chimeric N-terminal Escherichia coli C-terminal Rhodobacter sphaeroides FliG rotor protein supports bidirectional E. coli flagellar rotation and chemotaxis. J. Bacteriol. 187, 1695–1701 (2005).
Nicolau, D. V. Jr, Armitage, J. P. & Maini, P. K. Directional persistence and the optimality of run-and-tumble chemotaxis. Comput. Biol. Chem. 33, 269–274 (2009).
Wadhams, G. H., Martin, A. C. & Armitage, J. P. Identification and localization of a methyl-accepting chemotaxis protein in Rhodobacter sphaeroides. Mol. Microbiol. 36, 1222–1233 (2000).
Harrison, D. M., Skidmore, J., Armitage, J. P. & Maddock, J. R. Localization and environmental regulation of MCP-like proteins in Rhodobacter sphaeroides. Mol. Microbiol. 31, 885–892 (1999).
Wadhams, G. H. et al. TlpC, a novel chemotaxis protein in Rhodobacter sphaeroides, localizes to a discrete region in the cytoplasm. Mol. Microbiol. 46, 1211–1221 (2002).
Wadhams, G. H., Warren, A. V., Martin, A. C. & Armitage, J. P. Targeting of two signal transduction pathways to different regions of the bacterial cell. Mol. Microbiol. 50, 763–770 (2003). The demonstration that there are two separate chemotaxis clusters in R. sphaeroides.
Porter, S. L., Wadhams, G. H. & Armitage, J. P. In vivo and in vitro analysis of the Rhodobacter sphaeroides chemotaxis signaling complexes. Methods Enzymol. 423, 392–413 (2007).
Porter, S. L. & Armitage, J. P. Chemotaxis in Rhodobacter sphaeroides requires an atypical histidine protein kinase. J. Biol. Chem. 279, 54573–54580 (2004).
Poole, P. S. & Armitage, J. P. Role of metabolism in the chemotactic response of Rhodobacter sphaeroides to ammonia. J. Bacteriol. 171, 2900–2902 (1989).
Poole, P. S., Smith, M. J. & Armitage, J. P. Chemotactic signalling in Rhodobacter sphaeroides requires metabolism of attractants. J. Bacteriol. 175, 291–294 (1993).
Jacobs, M. H., Van Der Heide, T., Tolner, B., Driessen, A. J. & Konings, W. N. Expression of the gltP gene of Escherichia coli in a glutamate transport-deficient mutant of Rhodobacter sphaeroides restores chemotaxis to glutamate. Mol. Microbiol. 18, 641–647 (1995).
Storch, K. F., Rudolph, J. & Oesterhelt, D. Car: a cytoplasmic sensor responsible for arginine chemotaxis in the archaeon Halobacterium salinarum. EMBO J. 18, 1146–1158 (1999).
Bardy, S. L. & Maddock, J. R. Polar localization of a soluble methyl-accepting protein of Pseudomonas aeruginosa. J. Bacteriol. 187, 7840–7844 (2005).
Meier, V. M. & Scharf, B. E. Cellular localization of predicted transmembrane and soluble chemoreceptors in Sinorhizobium meliloti. J. Bacteriol. 191, 5724–5733 (2009).
Mauriello, E. M. F., Astling, D. P., Sliusarenko, O. & Zusman, D. R. Localization of a bacterial cytoplasmic receptor is dynamic and changes with cell-cell contacts. Proc. Natl Acad. Sci. USA 106, 4852–4857 (2009).
Wadhams, G. H., Martin, A. C., Warren, A. V. & Armitage, J. P. Requirements for chemotaxis protein localization in Rhodobacter sphaeroides. Mol. Microbiol. 58, 895–902 (2005).
Martin, A. C., Wadhams, G. H. & Armitage, J. P. The roles of the multiple CheW and CheA homologues in chemotaxis and in chemoreceptor localization in Rhodobacter sphaeroides. Mol. Microbiol. 40, 1261–1272 (2001).
Porter, S. L. & Armitage, J. P. Phosphotransfer in Rhodobacter sphaeroides chemotaxis. J. Mol. Biol. 324, 35–45 (2002).
Martin, A. C. et al. CheR- and CheB-dependent chemosensory adaptation system of Rhodobacter sphaeroides. J. Bacteriol. 183, 7135–7144 (2001).
Thompson, S. R., Wadhams, G. H. & Armitage, J. P. The positioning of cytoplasmic protein clusters in bacteria. Proc. Natl Acad. Sci. USA 103, 8209–8214 (2006).
Porter, S. L., Roberts, M. A. J., Manning C. S. & Armitage, J. P. A bifunctional kinase-phosphatase in bacterial chemotaxis. Proc. Natl Acad. Sci. USA 105, 18531–18536 (2008). The identification of a CheA protein with in-built phosphatase activity in R. sphaeroides.
Porter, S. L. et al. The CheYs of Rhodobacter sphaeroides. J. Biol. Chem. 281, 32694–32704 (2006).
Ferre, A., de la Mora, J., Ballado, T., Camarena, L. & Dreyfus, G. Biochemical study of multiple CheY response regulators of the chemotactic pathway of Rhodobacter sphaeroides. J. Bacteriol. 186, 5172–5177 (2004).
Scott, K. A. et al. Specificity of localization and phosphotransfer in the CheA proteins of Rhodobacter sphaeroides. Mol. Microbiol. 76, 318–330 (2010).
Ind, A. C. et al. An inducible expression plasmid for Rhodobacter sphaeroides and Paracoccus denitrificans. Appl. Environ. Microbiol. 75, 6613–6615 (2009).
Bell, C. H., Porter, S. L., Strawson, A., Stuart, D. I. & Armitage, J. P. Using structural information to change the phosphotransfer specificity of a two-component chemotaxis signalling complex. PLoS Biol. 8, e1000306 (2010). The identification of the specificity determinants for phosphotransfer from CheA-P to CheY.
Skerker, J. M. et al. Rewiring the specificity of two-component signal transduction systems. Cell 133, 1043–1054 (2008).
Tindall, M. J., Maini, P. K., Porter, S. L. & Armitage, J. P. Overview of mathematical approaches used to model bacterial chemotaxis II: bacterial populations. Bull. Math. Biol. 70, 1570–1607 (2008).
Tindall, M. J., Porter, S. L., Maini, P. K., Gaglia, G. & Armitage, J. P. Overview of mathematical approaches used to model bacterial chemotaxis I: the single cell. Bull. Math. Biol. 70, 1525–1569 (2008).
Tu, Y., Shimizu, T. S. & Berg, H. C. Modeling the chemotactic response of Escherichia coli to time-varying stimuli. Proc. Natl Acad. Sci. USA 105, 14855–14860 (2008).
Rao, C. V., Kirby, J. R. & Arkin, A. P. Design and diversity in bacterial chemotaxis: a comparative study in Escherichia coli and Bacillus subtilis. PLoS Biol. 2, e49 (2004).
Alon, U., Surette, M. G., Barkai, N. & Leibler, S. Robustness in bacterial chemotaxis. Nature 397, 168–171 (1999).
Tindall, M. J., Porter, S. L., Wadhams, G. H., Maini, P. K. & Armitage, J. P. Spatiotemporal modelling of CheY complexes in Escherichia coli chemotaxis. Prog. Biophys. Mol. Biol. 100, 40–46 (2009).
Tindall, M. J., Porter, S. L., Maini, P. K. & Armitage, J. P. Modeling chemotaxis reveals the role of reversed phosphotransfer and a bi-functional kinase-phosphatase. PLoS Comput. Biol. 6, e1000896 (2010).
Berry, R. M. & Armitage, J. P. Response kinetics of tethered Rhodobacter sphaeroides to changes in light intensity. Biophys. J. 78, 1207–1215 (2000).
Rasmussen, A. A., Porter, S. L., Armitage, J. P. & Sogaard-Andersen, L. Coupling of multicellular morphogenesis and cellular differentiation by an unusual hybrid histidine protein kinase in Myxococcus xanthus. Mol. Microbiol. 56, 1358–1372 (2005).
Rasmussen, A. A., Wegener-Feldbrugge, S., Porter, S. L., Armitage, J. P. & Sogaard-Andersen, L. Four signalling domains in the hybrid histidine protein kinase RodK of Myxococcus xanthus are required for activity. Mol. Microbiol. 60, 525–534 (2006).
Sourjik, V. & Schmitt, R. Phosphotransfer between CheA, CheY1, and CheY2 in the chemotaxis signal transduction chain of Rhizobium meliloti. Biochemistry 37, 2327–2335 (1998).
Roberts, M. et al. A model invalidation-based approach for elucidating biological signalling pathways, applied to the chemotaxis pathway in R. sphaeroides. BMC Syst. Biol. 3, 105 (2009).
Kristich, C. J. & Ordal, G. W. Bacillus subtilis CheD is a chemoreceptor modification enzyme required for chemotaxis. J. Biol. Chem. 277, 25356–25362 (2002).
Szurmant, H., Muff, T. J. & Ordal, G. W. Bacillus subtilis CheC and FliY are members of a novel class of CheY-P-hydrolyzing proteins in the chemotactic signal transduction cascade. J. Biol. Chem. 279, 21787–21792 (2004).
Chao, X. et al. A receptor-modifying deamidase in complex with a signaling phosphatase reveals reciprocal regulation. Cell 124, 561–571 (2006). A structural and biochemical study into the CheC–CheD adaptation circuit in B. subtilis.
Alexander, R. P., Lowenthal, A. C., Harshey, R. M. & Ottemann, K. M. CheV: CheW-like coupling proteins at the core of the chemotaxis signaling network. Trends Microbiol. 18, 494–503 (2010).
Kirby, J. R. Chemotaxis-like regulatory systems: unique roles in diverse bacteria. Annu. Rev. Microbiol. 63, 45–59 (2009). A survey of the chemosensory pathways that regulate processes other than chemotaxis.
Kirby, J. R. & Zusman, D. R. Chemosensory regulation of developmental gene expression in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 100, 2008–2013 (2003).
Zusman, D. R., Scott, A. E., Yang, Z. & Kirby, J. R. Chemosensory pathways, motility and development in Myxococcus xanthus. Nature Rev. Microbiol. 5, 862–872 (2007).
Berleman, J. E. & Bauer, C. E. Involvement of a Che-like signal transduction cascade in regulating cyst cell development in Rhodospirillum centenum. Mol. Microbiol. 56, 1457–1466 (2005).
Hickman, J. W., Tifrea, D. F. & Harwood, C. S. A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels. Proc. Natl Acad. Sci. USA 102, 14422–14427 (2005).
Meier, V. M., Muschler, P. & Scharf, B. E. Functional analysis of nine putative chemoreceptor proteins in Sinorhizobium meliloti. J. Bacteriol. 189, 1816–1826 (2007).
Hoff, W. D., Horst, M. A., Nudel, C. B. & Hellingwerf, K. J. Prokaryotic phototaxis. Methods Mol. Biol. 571, 25–49 (2009).
Packer, H. L. & Armitage, J. P. Behavioral responses of Rhodobacter sphaeroides to linear gradients of the nutrients succinate and acetate. Appl. Environ. Microbiol. 66, 5186–5191 (2000).
Tso, W.-W. & Adler, J. Negative chemotaxis in Escherichia coli. J. Bacteriol. 118, 560–576 (1974).
Romagnoli, S., Packer, H. L. & Armitage, J. P. Tactic responses to oxygen in the phototrophic bacterium Rhodobacter sphaeroides WS8N. J. Bacteriol. 184, 5590–5598 (2002).
Shaw, C. H., Ashby, A. M., Brown, A., Royal, C. & Loake, G. J. virA and virG are the Ti-plasmid functions required for chemotaxis of Agrobacterium tumefaciens towards acetosyringone. Mol. Microbiol. 2, 413–417 (1988).
Seymour, J. R., Simo, R., Ahmed, T. & Stocker, R. Chemoattraction to dimethylsulfoniopropionate throughout the marine microbial food web. Science 329, 342–345 (2010).
Alexandre, G. Coupling metabolism and chemotaxis-dependent behaviours by energy taxis receptors. Microbiology 156, 2283–2293 (2010).
Edwards, J. C., Johnson, M. S. & Taylor, B. L. Differentiation between electron transport sensing and proton motive force sensing by the Aer and Tsr receptors for aerotaxis. Mol. Microbiol. 62, 823–837 (2006).
Rebbapragada, A. et al. The Aer protein and the serine chemoreceptor Tsr independently sense intracellular energy levels and transduce oxygen, redox, and energy signals for Escherichia coli behavior. Proc. Natl Acad. Sci. USA 94, 10541–10546 (1997).
Watts, K. J., Johnson, M. S. & Taylor, B. L. Structure-function relationships in the HAMP and proximal signaling domains of the aerotaxis receptor Aer. J. Bacteriol. 190, 2118–2127 (2008).
Hou, S. et al. Myoglobin-like aerotaxis transducers in Archaea and Bacteria. Nature 403, 540–544 (2000).
Jiang, Z. Y. & Bauer, C. E. Component of the Rhodospirillum centenum photosensory apparatus with structural and functional similarity to methyl-accepting chemotaxis protein chemoreceptors. J. Bacteriol. 183, 171–177 (2001).
Guvener, Z. T. & Harwood, C. S. Subcellular location characteristics of the Pseudomonas aeruginosa GGDEF protein, WspR, indicate that it produces cyclic-di-GMP in response to growth on surfaces. Mol. Microbiol. 66, 1459–1473 (2007).
Hickman, J. W. & Harwood, C. S. Identification of FleQ from Pseudomonas aeruginosa as a c-di-GMP-responsive transcription factor. Mol. Microbiol. 69, 376–389 (2008).
Berleman, J. E., Scott, J., Chumley, T. & Kirby, J. R. Predataxis behavior in Myxococcus xanthus. Proc. Natl Acad. Sci. USA 105, 17127–17132 (2008).
Platzer, J., Sterr, W., Hausmann, M. & Schmitt, R. Three genes of a motility operon and their role in flagellar rotary speed variation in Rhizobium meliloti. J. Bacteriol. 179, 6391–6399 (1997).
Garrity, L. F. & Ordal, G. W. Activation of the CheA kinase by asparagine in Bacillus subtilis chemotaxis. Microbiology 143, 2945–2951 (1997). The demonstration that chemotactic signalling in B. subtilis is reversed with respect to E. coli , with increases in attractant concentration activating CheA autophosphorylation.
Guvener, Z. T., Tifrea, D. F. & Harwood, C. S. Two different Pseudomonas aeruginosa chemosensory signal transduction complexes localize to cell poles and form and remould in stationary phase. Mol. Microbiol. 61, 106–118 (2006).
Szurmant, H., Bunn, M. W., Cannistraro, V. J. & Ordal, G. W. Bacillus subtilis hydrolyzes CheY-P at the location of its action: the flagellar switch. J. Biol. Chem. 278, 48611–48616 (2003).
Berleman, J. E. & Bauer, C. E. A che-like signal transduction cascade involved in controlling flagella biosynthesis in Rhodospirillum centenum. Mol. Microbiol. 55, 1390–1402 (2005).
Ulrich, L. E. & Zhulin, I. B. The MiST2 database: a comprehensive genomics resource on microbial signal transduction. Nucleic Acids Res. 38, D401–D407 (2010).
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This research was funded by the UK Biotechnology and Biological Sciences Research Council.
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DATABASES
Protein Data Bank
FURTHER INFORMATION
Glossary
- Two-component signalling pathway
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A bacterial signalling system comprising histidine protein kinases and response regulators; these pathways regulate diverse processes, including virulence, development and chemotaxis.
- Chemoeffector
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A collective term for an attractant or repellent.
- Histidine protein kinase
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The sensor in a two-component signal transduction pathway. These kinases autophosphorylate at a conserved histidine residue using ATP as the phosphodonor. The rate at which they autophosphorylate is controlled by sensory stimuli. Following autophosphorylation, the kinase serves as a phosphodonor for a specific response regulator. CheA is the chemotaxis histidine protein kinase.
- Response regulator
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A protein containing a receiver domain that is phosphorylated on an aspartate residue by a histidine protein kinase. Phosphorylation of the receiver domain induces a conformational change that activates the response regulators. Signal termination is achieved by hydrolysis of the aspartyl-phosphate bond, catalysed by a phosphatase in some systems.
- Autophosphorylation
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The process in which a histidine protein kinase phosphorylates itself using ATP as the phosphodonor. Typically, the rate of this process is controlled by environmental stimuli.
- Signal termination
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The removal of the phosphoryl groups from the signalling pathway. This is achieved by hydrolysis of the aspartyl-phosphate bonds in the phosphorylated response regulators.
- Adaptation
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The process by which the signalling state of the chemotaxis pathway is reset to the background concentration of chemoeffectors experienced in the recent past. An adapted cell will have an intermediate tumble bias, allowing cells to respond either negatively or positively to future changes in chemoeffector concentration.
- PAS domain
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A domain named owing to its conservation in the protein families period circadian protein (PER), aryl hydrocarbon receptor nuclear translocator (ARNT) and single-minded (SIM). PAS domains bind a diverse range of small-molecule ligands (for example, haem and FAD) and are often involved in redox and light sensing.
- Ordinary differential equation (ODE) mathematical model
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As used here, a set of mathematical equations that represents the changes in the phosphorylation levels of the chemotaxis proteins as a function of time.
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Porter, S., Wadhams, G. & Armitage, J. Signal processing in complex chemotaxis pathways. Nat Rev Microbiol 9, 153–165 (2011). https://doi.org/10.1038/nrmicro2505
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DOI: https://doi.org/10.1038/nrmicro2505
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